ISSN (impresso) 0103-5657 ISSN (on-line) 2178-7875 Revista Brasileira de Ornitologia

Volume 19 Número 4 www.ararajuba.org.br/sbo/ararajuba/revbrasorn Dezembro 2011

Publicada pela Sociedade Brasileira de Ornitologia São Paulo - SP Revista Brasileira de Ornitologia, 19(4), 535‑538 nOTA Dezembro de 2011

Foraging behavior of Hudsonian Godwit Limosa haemastica (Charadriiformes, Scolopacidae) in human-disturbed and undisturbed occasions in the Atlantic coast of

César Cestari1,2

1. Programa de Pós-Graduação em Zoologia, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Campus de Rio Claro. CEP 13506‑900, Rio Claro, SP, Brasil. 2. Current address: Departamento de Zoologia, Universidade Estadual Paulista “Júlio de Mesquita Filho” (UNESP), Campus de Rio Claro. CEP 13506‑900, Rio Claro, SP, Brasil. E‑mail: [email protected]

Recebido em: 04/03/2011. Aceito em: 01/09/2011.

Resumo: Comportamento de forrageio do maçarico-de-bico-virado Limosa haemastica (Aves, Scolopacidae) em ocasiões com perturbação e sem perturbação humana na costa Atlântica do Brasil. O maçarico-de-bico-virado, Limosa haemastica é considerado uma das aves pernaltas mais pouco estudadas que se reproduzem na América do Norte. Durante a migração, esta espécie utiliza poucas escalas até alcançar áreas de invernada no sul da América do Sul. Desta forma, estudos biológicos no decorrer de sua rota de migração são escassos. O foco deste artigo foi analisar o comportamento de forrageio de três indivíduos migrantes do maçarico-de-bico-virado que fizeram escala em áreas de entre-marés da costa sul do estado de São Paulo. Eu utilizei uma câmera digital para filmar e quantificar precisamente as técnicas de forrageio, o tempo de forrageio em hábitats e as distâncias percorridas pelas aves. Estas mesmas variáveis foram quantificadas em situações com e sem perturbação causadas por pessoas andando próximas das aves em forrageio. Os maçaricos-de-bico-virado utilizaram mais freqüentemente a técnica de “bicar superficialmente” em solo do que a técnica de “enterrar o bico” em solo. Eles forragearam a maior parte do tempo em solo úmido; alimentaram-se em média 31.91 ± 15.48 vezes por minuto e andaram em média de 4.40 ± 2.29 m por minuto. Os maçaricos-de-bico-virado andaram distâncias similares em ocasiões com perturbação e sem perturbação humana, porém eles forragearam menos em ocasiões com perturbação. Os resultados obtidos ressaltam a vulnerabilidade desta espécie durante os períodos de coexistência com humanos em locais com atividades recreação durante a migração.

Palavras-Chave: América do Sul; ave neártica; escala filmagem; migração.

Key-Words: South America; Nearctic bird; stopover; filming, migration.

The Hudsonian Godwit Limosa haemastica breeds The Hudsonian Godwit is one of the most poorly from May through July in the tundra of North America studied North America-breeding shorebird. Basic infor- from Alaska to the Hudson Bay, EUA, and spend the non- mation of the species, such as migration routes, breed- breeding season in southern South America. While in the ing and non-breeding places, and precise population es- south hemisphere, godwits rely on a few, very important timates require research (Senner 2010). Previous studies wintering sites (Senner 2010). The majority of individu- in South America have presented data on relative abun- als concentrate on Chiloé Island, southern Chile and in dance, habitat use, and feeding ecology of godwits (e.g., Tierra del Fuego, southern tip of Argentina/Chile (Mor- Hayes and Fox 1991, Blanco 1998, Brayton and Sche- rison and Ross 1989, Andres et al. 2009, Senner 2010). neider 2000, Hernández et al. 2008, Andres et al. 2009, In Brazil, godwits mainly stop at Lagoa do Peixe, Lizarralde et al. 2010). In this paper, I focus on the for- state of Rio Grande do Sul while migrating to their breed- aging behavior of three Hudsonian Godwits that used ing grounds (Morrinson and Ross 1989, Belton 1994). In stopover sites on the southern coast of the state of São other states (e.g., Amapá, Sergipe, São Paulo, Paraná, and Paulo (southeast Brazil) during their southbound migra- ), the species has been recorded as indi- tion. Additionally, I compare feeding rates and walking viduals or small groups, especially along the Atlantic coast distance of foraging godwits between sporadic periods of (Olmos and Silva 2001, Willis and Oniki 2003, Barbieri human disturbance (mainly caused by tourists on foot) 2007). and periods without disturbance. Several studies indicate 536 Foraging behavior of Hudsonian Godwit Limosa haemastica (Charadriiformes, Scolopacidae) in human-disturbed and undisturbed occasions in the Atlantic coast of Brazil César Cestari that human recreational activities affect the behavior of in the water to probe. In addition to the feeding rate, migratory birds using coastal environments (e.g., Burger the time and the distance walked by individuals while 1981, Burger and Gochfeld 1991, Burger et al. 2004). foraging on the wet sand (saturated sand or with surface Therefore, I hypothesize that godwits decrease their feed- layer of water) and dry sand (without wetness) were also ing rate and increase their distance walked while foraging recorded. The walking distance was calculated using the due to human disturbance. average distance of the species pace (= 4.60 cm, estimated Hudsonian Godwits were found in two inter- from footprints in wet sand) multiplied by the number tidal sites: Grajaúna River at Juréia Ecological Station of steps. (24°31.4’S; 47°11.1’W) and a beach at Itanhaém munici- I used a digital Sony DSC H50 camera to precisely pality (24°13.3’S; 46°51.1’W). During the first occasion record foraging godwits. To avoid influence birds behav- (19‑20 October 2010), one individual foraged in a tem- ior, all the recordings were taken at distance about 10 m. porary lake connected with the Grajaúna river mouth. The above ecological traits (feeding rate, foraging time in During the second occasion (15‑17 November 2010), each habitat, and walking distance) were later quantified two individuals foraged on the shoreline of a severely dis- for further analysis. I defined a sample as recording of turbed sandy beach, mainly due to tourists walking along one minute of foraging. The samples of time foraging and the beach. Both areas have soft sandy sediments, low de- feeding rate with different foraging techniques between clivity (4‑6°) and tidal influence of 87 ± 9 m. habitats (wet and dry sand) were compared using a Stu- The Hudsonian Godwit is a medium-sized wader dent’s T‑test with the Bioestat 4.0 software (Ayres et al. (37‑42 cm in length) with a long, slightly up-curved bill 2004). The same statistical analysis was used to compare from the middle to the tip (culmen of 7.35‑7.55 cm in the species’ ecological traits (feeding rate and walking males, and 8.8‑9.0 cm in females; Sutton 1968, Hayman distance) during instances of human disturbance and et al. 1986). This bill length enables the bird to capture without disturbance. Human disturbance was defined as prey at a variety of depths. According to Baker (1977), when a person, or group of people, approached a bird to Kinsella et al. (2007) and Hernández et al. (2008), god- within less than five meters. wits may feed primarily on benthic invertebrates from Hudsonian Godwits spent more time foraging coastal environments. Hence, considering the above cir- on wet (50.76 ± 16.72 s) than on dry sand habitats cumstances, I quantified the feeding rate per min of the (9.19 ± 16.68 s) (t = ‑12; df = 92; P < 0.0001) in a total three foraging godwits and detailed the foraging tactic of 93 min of recordings. They fed 31.91 ± 15.48 times they used to capture prey, according to the proportion and walked a straight distance of 4.40 ± 2.29 m per min. of their bill inserted into soil substrate: ‘Pecking’ was de- Pecking technique was used more than probing on both fined as fast movement of the bill toward the sand sur- wet (t = 2.13; df = 92; P = 0.03) and dry sand habitats face to capture prey. ‘Mid-probing’ was defined as when (t = 4.54; df = 92; P < 0.0001) (Figure 1). Birds walked the bird buried its bill in the sand up to half its length a similar distance when foraging with and without hu- (3.5‑4.5 cm). ‘Deep-probing’ was defined as when the man disturbance (t = ‑0.50; df = 91; P = 0.616), but bird buried its bill in the sand more than a half of its total length. In the latter, a bird may insert its entire head

Figure 1: Feeding rate (per minute) using different foraging tech- Figure 2: Walking distance and feeding rate of godwits that foraged niques performed by godwits in wet sand and dry sand habitats from with and without human-disturbance along the southern coast of the the southern coast of the São Paulo State, Brazil. São Paulo State, Brazil.

Revista Brasileira de Ornitologia, 19(4), 2011 Foraging behavior of Hudsonian Godwit Limosa haemastica (Charadriiformes, Scolopacidae) in 537 human-disturbed and undisturbed occasions in the Atlantic coast of Brazil César Cestari they foraged less during periods of human disturbance in Argentina and Chile during the boreal winter (Andres (t = 2.32; df = 91; P = 0.0226) (Figure 2). et al. 2009, Senner 2010). It also indicates the possibility Hudsonian Godwits spent most of their time for- that these birds are habituating to humans (Nisbet 2000). aging on wet sand, sometimes in shallow water condi- Unhealthy birds are less efficient at responding to tions. Their long bill and legs enable them to forage in up human disturbances (Gill et al. 2001a). However, some to 16.5 cm of water, presumably an unsuitable foraging variations in bird behavior may also be confounded by condition for other shorebirds with shorter bills and legs. prey abundance in the study area (Gill et al. 2001b). For instance, according to Brayton and Schneider (2000), Thus, there is also the possibility that healthy godwits godwits continued feeding on benthic invertebrates af- were foraging on patches of the beach with high prey ter the tide rose, while shorter-billed shorebirds, such as availability, and a prompt move to another patch as a hu- Calidris sandpipers, stopped feeding and flew to higher man approaches might be unrewarding. McArthur and foraging sites. Pianka (1966) assumed that an activity should be en- Studies on predator-prey relationships have shown gaged in for as long as the resulting gain in time spent per that deeply buried prey are less accessible to shorebirds unit of food exceeds the loss. During all the recordings, (Waninck and Zwars 1985, Piersma et al. 1993). Prob- the godwits did not show any sign of unhealthiness. As ably, their long bill enables godwits to search for prey at a a result, the first and third hypotheses mentioned above variety of soil depths. According to Brayton and Schnei- may better explain the lack of difference in the distance der (2000), amphipods, isopods, and ostracods were of- walked between godwits in situations with and without ten found near the soil surface, while polychaetes were human disturbance. found deeper in the soil. Unfortunately, even after careful Studies of the foraging behavior of Hudsonian God- analysis of film recordings, I was unable to identify prey, wit in areas with human disturbance are scarce. The pre- due to their tiny sizes and fast movements of godwits. liminary results of this study showed that godwits fed less Studies of fecal droppings in Argentina pointed out that frequently during short periods of coexistence with hu- godwits mainly prey on bivalves (especially Darina sole‑ mans. Future studies involving the quality of habitats in noids) and polychaetes (Hernández et al. 2008; Lizarralde terms of degree of human disturbances and the quantity et al. 2010). and energetic value of godwit’s prey are welcome. The energetic costs of foraging by different tech- niques can differ considerably among migratory birds (Evans 1976). The fast and short-period movements of Acknowledgements pecking more employed by godwits resulted in a high- er feeding rate per minute than the probing technique. I thank my family for love support. I am also indebted with all Thus, assuming that prey from different soil deeps have the staff of Juréia Ecological Station that facilitated my work in the similar energetic value, pecking may be important be- region and Alaine A. Ball for English revisions. CC received research cause birds may maximize energy and continue migration grants from the Brazilian Research Council (CNPq). to reach prime non-breeding grounds in Argentina and Chile (Kokko 1999, Senner 2010). References Human recreational activities reduce the foraging time of migratory birds (see Burger and Gochfeld 1991, Andrés, B. A.; Johnson, J. A.; Valenzuela, J.; Morrison; R. I. G.; Yasué et al. 2008). As expected, the godwits showed Espinosa, L. A. e Ross, R. K. (2009). Estimating eastern Pacific a decrease in the feeding rate when disturbed by walk- coast populations of Whimbrels and Hudsonian Godwits, with an ing humans but they did not move (walk) more in these emphasis on Chiloé Island, Chile. Waterbirds, 32:216‑224. situations. Three non exclusive hypotheses might explain Ayres, M. M.; Ayres, J. R.; Ayres, D. L. e Santos, A. S. (2004). 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Revista Brasileira de Ornitologia, 19(4), 2011